Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-26T13:16:56.408Z Has data issue: false hasContentIssue false

Association between p34cdc2 levels and meiotic arrest in pig oocytes during early growth

Published online by Cambridge University Press:  26 September 2008

Yuji Hirao
Affiliation:
Kobe University and National Institute of Animal Industry, Ibaraki, Japan, and The Babraham Institute, Cambridge, UK.
Youki Tsuji
Affiliation:
Kobe University and National Institute of Animal Industry, Ibaraki, Japan, and The Babraham Institute, Cambridge, UK.
Takashi Miyano*
Affiliation:
Kobe University and National Institute of Animal Industry, Ibaraki, Japan, and The Babraham Institute, Cambridge, UK.
Akira Okano
Affiliation:
Kobe University and National Institute of Animal Industry, Ibaraki, Japan, and The Babraham Institute, Cambridge, UK.
Masashi Miyake
Affiliation:
Kobe University and National Institute of Animal Industry, Ibaraki, Japan, and The Babraham Institute, Cambridge, UK.
Seishiro Kato
Affiliation:
Kobe University and National Institute of Animal Industry, Ibaraki, Japan, and The Babraham Institute, Cambridge, UK.
Robert M. Moor
Affiliation:
Kobe University and National Institute of Animal Industry, Ibaraki, Japan, and The Babraham Institute, Cambridge, UK.
*
T. Miyano, Department of Animal Breeding and Reproduction, Faculty of Agriculture, Kobe University, Nada-ku, Kobe 657, Japan. Telephone: 078 803 0621. Fax: 073 803 0622. e-mail: [email protected].

Summary

The molecules involved in determining meiotic competence were determined in porcine oocytes isolated from preantral and antral follicles of different sizes. Oocytes isolated from preantral follicles had a mean diameter of 78 μm, contained diffuse filamentous chromatin in the germinal vesicle and were incapable of progressing from the G2 to the M phase of the cycle even after 72 h in culture. Oocytes from early antral follicles had a mean diameter of 105 μm, showed a filamentous chromatin configuration and about half resumed meiosis but arrested at metaphase I (MI) when cultured. Oocytes from mid-antral (3–4 mm) and large antral follicles (5–6 mm) had mean oocyte diameters of 115 and 119 μm respectively, contained condensed chromatin around the nucleolus and progressed to metaphase II (MII) in 48% and 93% of instances respectively. Analysis of p34cdc2, the catalytic subunit of maturation promoting factor (MPF), by immunoblotting indicates that the inability of small (78 μm) oocytes to resume meiosis is due, at least in part, to inadequate levels of the catalytic subunit of MPF. On the other hand, the inability of intermediate-sized (105 μm) oocytes from antral follicles to complete the first meiotic division by progressing beyond MI appears not to be limited by levels of p34cdc2, which are maximal by this stage. We postulate that an inadequacy of molecules other than p34cdc2 limits progression of MI to MII; the acquisition of these molecules during the final stages of growth may be correlated with the formation of the perinucleolar chromatin rim in the germinal vesicle.

Type
Article
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bjerrum, O.J. & Schafer-Nielsen, C. (1986). Buffer systems and transfer for semidry electroblotting with a horizontal apparatus. In Analytical Electrophoresis, Duns, M.J., 315–27. Weinheim: Verlag Chemie.Google Scholar
Bornslaeger, E.A., Mattei, P.M. & Schultz, R.M. (1988). Protein phosphorylation in meiotically competent and incompetent mouse oocytes. Mol. Reprod. Dev. 1, 1925.CrossRefGoogle ScholarPubMed
Chesnel, F. & Eppig, J.J. (1995). Synthesis and accumulation of p34cdc2 and cyclin B in mouse oocytes during acquisition of competence to resume meiosis. Mol. Reprod. Dev. 40, 503–8.CrossRefGoogle ScholarPubMed
Christmann, L., Jung, T. & Moor, R.M. (1994). MPF components and meiotic competence in growing pig oocytes. Mol. Reprod. Dev. 38, 8590.CrossRefGoogle ScholarPubMed
Crozet, N., Motlik, J. & Szöllösi, D. (1981). Nucleolar fine structure and RNA synthesis in porcine oocytes during the early stages of antrum formation. Biol. Cell 41, 3542.Google Scholar
Edwards, R.G. (1965). Maturation in vitro of mouse, sheep, cow, pig, Rhesus monkey and human ovarian oocytes. Nature 208, 349–51.CrossRefGoogle ScholarPubMed
Fulka, J. Jr & Moor, R.M. (1993). Noninvasive chemical enucleation of mouse oocytes. Mol. Reprod. Dev. 34, 427–30.CrossRefGoogle ScholarPubMed
Fulka, J. Jr, Jung, T. & Moor, R.M. (1992). The fall of biological maturation promoting factor (MPF) and histone H1 kinase activity during anaphase and telophase in mouse oocytes. Mol. Reprod. Dev. 32, 378–82.CrossRefGoogle ScholarPubMed
Fulka, J. Jr, Moor, R.M. & Fulka, J. (1994). Sister chromatid separation and the metaphase-anaphase transition in mouse oocytes. Dev. Biol. 165 410–17.CrossRefGoogle ScholarPubMed
Gavin, A.C., Tsukitani, Y. & Schorderet-Slatkine, S. (1991). Induction of M-phase entry of prophase-blocked mouse oocytes through microinjection of okadaic acid, a specific phosphatase inhibitor. Exp. Cell Res. 192, 7581.CrossRefGoogle ScholarPubMed
Hampl, A. &Eppig, J.J. (1995). Analysis of mechanism(s) of metaphase I arrest in maturing mouse oocytes. Development 121, 925–33.CrossRefGoogle ScholarPubMed
Hashimoto, N. & Kishimoto, T. (1988). Regulation of meiotic metaphase by cytoplasmic maturation-promoting factor during mouse oocyte maturation. Dev. Biol. 126, 242–52.CrossRefGoogle ScholarPubMed
Jelinkova, L., Kubelka, M., Motlik, J. & Guerrier, P. (1994). Chromatin condensation and histone H1 kinase activity during growth and maturation of rabbit oocytes. Mol. Reprod. Dev. 37, 210–15.CrossRefGoogle ScholarPubMed
Laemmli, U.K. (1970). Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227,680–5.CrossRefGoogle ScholarPubMed
Mattioli, M., Galeati, G., Bacci, M.L. & Barboni, B. (1991). Changes in maturation-promoting activity in the cytoplasm of pig oocytes throughout maturation. Mol. Reprod. Dev. 30, 119–25.CrossRefGoogle ScholarPubMed
McKim, K.S., Jang, J.K., Theurkauf, W.E. & Hawley, R.S. (1993). Mechanical basis of meiotic metaphase arrest. Nature 362, 364–6.CrossRefGoogle ScholarPubMed
Meyerson, M., Enders, G.H., Wu, C.-L, Su, L.-K, Gorka, C., Nelson, C., Harlow, E. & Tsai, L.-H (1992). A family of human cdc2-related protein kinases. EMBO J. 11, 2909–17.CrossRefGoogle ScholarPubMed
Moor, R.M. & Trounson, A.O. (1977). Hormonal and follicular factors affecting maturation of sheep oocytes in vitro and subsequent developmental capacity. J. Reprod. Fertil. 49, 101–9.CrossRefGoogle ScholarPubMed
Moor, R.M., Jung, T., Miyano, T. & Baker, P. (1992). Cyclin and p34cdc2 kinase activity in pig oocyte during the G2-to M-phase transition. In Gonadal Development and Function, Hillier, S.G., pp. 8598. New York: Serono Symposium Publications, Raven Press.Google Scholar
Motlik, J. & Fulka, J. (1976). Breakdown of the germinal vesicle in pig oocytes in viva and in vitro. J. Exp. Zool. 198,155–62.Google Scholar
Motlik, J. & Kubelka, M. (1990). Cell-cycle aspects of growth and maturation of mammalian oocytes. Mol. Reprod. Dev. 27, 366–75.CrossRefGoogle ScholarPubMed
Motlik, J., Crozet, N. & Fulka, J. (1984). Meiotic competence in vitro of pig oocytes isolated from early antral follicles. J. Reprod. Fertil. 72, 323–8.CrossRefGoogle ScholarPubMed
Murray, A.W. (1992). Creative blocks: cell-cycle checkpoints and feedback controls. Nature 359, 599604.CrossRefGoogle ScholarPubMed
Murray, A.W. & Hunt, T. (1993). Mitosis. In The Cell Cycle: An Introduction, Murray, A. &Hunt, T., pp.6688. New York: W.H. Freeman.Google Scholar
Sato, E., Matsuo, M. & Miyamoto, H. (1990). Meiotic maturation of bovine oocytes in vitro: improvement of meiotic competence by dibutyryl cyclic adenosine 3',5'-monophosphate. J. Anim. Sci. 68, 1182–7.CrossRefGoogle ScholarPubMed
Schultz, R.M., Letourneau, G.E. & Wassarman, P.M. (1979). Program of early development in the mammal: changes in the patterns and absolute rates of tubulin and total protein synthesis during oocyte growth in the mouse. Dev. Biol. 73, 120–33.CrossRefGoogle ScholarPubMed
Sorensen, R.A. & Wassarman, P.M. (1976). Relationship between growth and meiotic maturation of the mouse oocyte. Dev. Biol. 50, 531–6.CrossRefGoogle ScholarPubMed
Surana, U., Amon, A., Dowzer, C., McGrew, J., Byers, B. & Nasmyth, K. (1993). Destruction of the CDC28/CLB mitotic kinase is not required for the metaphase to anaphase transition in budding yeast. EMBO J. 12, 1969–78.CrossRefGoogle Scholar
Wassarman, P.M. (1988). The mammalian ovum. In The Physiology of Reproduction,Knobil, E. & Neil, J., pp. 69102. New York: Raven Press.Google Scholar
Wickramasinghe, D., Ebert, K.M. & Albertini, D.F. (1991). Meiotic competence acquisition is associated with the appearance of M-phase characteristics in growing mouse oocytes. Dev. Biol. 143, 162–72.CrossRefGoogle ScholarPubMed
Yamashita, M., Yoshikuni, M., Hirai, T., Fukada, S. & Nagahama, Y. (1991). A monoclonal antibody against the PSTAIR sequence of p34cdc2, catalytic subunit of maturation-promoting factor and key regulator of the cell cycle. Dev. Growth Differ. 33, 617–24.CrossRefGoogle ScholarPubMed